Collaborative Research: Symbiosis as a fulcrum in a rapidly warming world

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Climate change is creating unprecedented challenges for Earth’s inhabitants. It is critical to understand how rising temperatures affect the diversity and distributions of organisms. However, predicting organismal responses to climate change is difficult, because species interactions are impacted differently than individual species. Moreover, these predictions are further complicated because species interactions often involve ‘hidden’ microbes called symbionts, which appear especially vulnerable to climate change. This is exemplified by the photosynthesizing symbionts of marine corals, which are expelled during ocean warming. Less is known about climate impacts on symbiont-mediated species interactions in terrestrial systems. Unique opportunities to study this phenomenon occur using tractable aphid models with their well-characterized protective symbioses. Aphids are plant-feeding insects and important agricultural pests, which carry bacterial symbionts that protect them against pathogens and parasites. Prior work showed that most strains of a widespread anti-parasite symbiosis failed to protect aphids at warmer temperatures. But other strains of this symbiont, and from a second non-essential symbiont species, provided aphids with tolerance to high temperatures in the absence of parasites– plausibly by rescuing a third symbiont species required for aphid survival. Combining biological experiments with molecular biology, microscopy, genomics and gene expression studies, the PIs will study mechanisms of temperature-mediated symbiont failure and, conversely, the potential for symbiont-mediated climate resilience. Insects are the most diverse animal group, and most are symbiotic, so findings from aphids readily generalize to most terrestrial animals. This award supports the training and professional development of high school, undergraduate, graduate researchers, and includes community outreach events. Predicting organismal responses to climate change is difficult because species interactions are impacted differently than individual species. A further complication is that interactions among multicellular eukaryotes are often mediated by microbial partners, which appear especially vulnerable to thermal stress. Climate impacts on microbe-mediated species interactions will be investigated using a highly-tractable aphid model system with defensive symbioses that have been well-characterized at genotypic and phenotypic levels. Prior work showed that most strains of a widespread anti-parasitoid symbiont, Hamiltonella, fail to protect aphids at warmer temperatures. Using common strains derived from natural populations, cage experiments will test hypotheses that 1) fluctuating temperatures maintain thermally-relevant genetic variation in Hamiltonella, while 2) monolithic exposure to hot temperatures without parasitoids selects for strains conferring thermal tolerance, and 3) challenge with both warm temperatures and parasitoids selects for strains providing thermally-robust protection. Additional assays will define the upper limits of Hamiltonella function, and whether another symbiont, Serratia, replaces Hamiltonella in the hottest locales. To understand mechanisms of symbiont failure and resilience, relevant genomes will be sequenced coupled with assays examining symbiont titers in response to thermal stress, heat lability of toxins, and whether thermal tolerance occurs via rescue of the obligate nutritional symbiont Buchnera. This research enhances understanding of climate impacts on the ubiquitous heritable symbioses of insects, with implications for the many beneficial services provided, and threats to human health and agriculture posed.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.